Applied Soil Ecology 76 (2014) 78–86 Contents lists available at ScienceDirect Applied Soil Ecology journa l homepage: www.elsevier.com/locate/apsoil Inter- and intraspecific functional variability of tropical arbuscular mycorrhizal fungi isolates colonizing corn plants a b c Cândido Barreto de Novais , Wardsson Lustrino Borges , Ederson da Conceic¸ ão Jesus , c d,∗ Orivaldo José Saggin Júnior , José Oswaldo Siqueira a Universidade Federal de Lavras, DCS-Laboratório de Microbiologia do Solo, Caixa Postal 3037, CEP 37200-000, Lavras, MG, Brazil b ◦ Embrapa Amapá, Rodovia Juscelino Kubitschek, km 5, N 2600, CEP 68903-419, Macapá, AP, Brazil c Embrapa Agrobiologia, Rodovia BR 465, km 7, Seropédica, RJ, CEP: 23891-000, Brazil d ◦ Vale Technological Institute-Mining, Rua Antonio de Albuquerque, 271 9 andar, 30112010 Belo Horizonte, MG, Brazil a r a t i b s c l t r e a i n f o c t Article history: For a single plant species under the same environmental conditions, the interaction with arbuscular Received 2 August 2013 mycorrhizal fungi (AMF) and their contribution to plant growth varies among AMF isolates, with both Received in revised form inter and intraspecific variability. The present study evaluated the functional variability of 41 isolates of 10 December 2013 20 species and eight genera of AMF for root colonization, growth promotion, and P uptake of corn and Accepted 18 December 2013 observed the relationship of this functional variability with the isolates genetic variability revealed by PCR-RFLP analysis. All the isolates abundantly colonized the corn roots, but only 23 promoted higher Keywords: shoot dry mass and P leaf content. The cluster analysis based on functional variability data separated the RFLP isolates Acaulospora morrowiae (Am2), Acaulospora sp. (Aca), A. colombiana (Ac3, Ac4, and Ac5), Gigaspora Geographical isolates Glomus albida (Gia1), Gi. margarita (Gim4 and Gim5), Gi. rosea (Gir), Rhizophagus clarus (Rc2, Rc3, Rc4, Rc5, and Gigaspora Rc6), Claroideoglomus etunicatum (Ce4), R. manihotis (Rm), Scutellospora calospora (Sc), S. heterogama Acaulospora (Sh2, Sh3, Sh4, and Sh5) and S. pellucida (Sp3) from the others at the distance of 80% functional similarity. These were considered efficient in promoting functional symbiosis in corn while the other isolates were considered inefficient. The cluster analysis obtained by the PCR-RFLP technique was partly coherent with the species classification based on spore morphology. The isolates of R. clarus fell into one cluster and the isolates of the Gigaspora and Scutellospora genera (Gigasporaceae family) were clustered in a second cluster, without the ability to separate the species of these genera. © 2014 Elsevier B.V. All rights reserved. 1. Introduction documented, but the mechanisms that regulate these interactions and effects are poorly understood. This leaves doubt about the role The arbuscular mycorrhizal fungi (AMF) form symbiotic rela- of AMF in crop yields and recuperation of degraded ecosystems tionships with the majority of land plant species and are distributed hampering the definition of strategies for the application of these throughout the tropics. This association is characterized by the pen- fungi. etration of the fungal mycelium between and within the cells of the At present 230 AMF species are known (Schüßler and Walker, radicular cortex, without causing visible morphological change to 2010), a number considered low compared to the number of plant the naked eye, but that modifies the plant’s physiology, enhancing species with which these fungi can associate. This situation induces its capacity to absorb nutrients from the soil, especially those with the view that AMF form a homogenous group of symbionts in which low soil mobility such as phosphorus. For the same plant species, all the species perform identical biological functions in the ecosys- the effects and contribution of AMF vary according to the fungal tem (Husband et al., 2002). isolates, reflected in differences in the symbiotic efficiency of the The use of molecular techniques based on PCR-RFLP (poly- fungus (van der Heijden and Kuyper, 2001). This variation is well merase chain reaction – restriction fragment length polymor- phism) has allowed verification that the AMF community in the rhizosphere varies among plant species (Babu and Reddy, 2011; Martínez-García and Pugnaire, 2011) and among soils with differ- ∗ Corresponding author. Tel.: +55 31 3194 4083. ent concentrations of nutrients (Martinez-García et al., 2011). It has E-mail addresses: [email protected] (C.B. de Novais), been found that the community variability is greater in the rhizo- [email protected], [email protected] (W.L. Borges), sphere than in the roots (Martinez-García et al., 2011; Miras-Avalos [email protected] (E.d.C. Jesus), [email protected] (O.J.S. Júnior), [email protected] (J.O. Siqueira). et al., 2011), suggesting some degree of preference or specificity. 0929-1393/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.apsoil.2013.12.010 C.B. de Novais et al. / Applied Soil Ecology 76 (2014) 78–86 79 According to Wagg et al. (2011), due to the seemingly limitless host plant’s nutrition and growth. The difference in symbiotic per- possibilities for complementarity or selection effect, it is difficult, if formance observed among different AMF isolates is considered as not impossible, to determine all the functional and resource-based a measure of the functional variability of mycosymbionts (Pouyu- niches that each AMF species within a more AMF-rich commu- Rojas et al., 2006). Corn shows high growth rate, high uptake of nity can occupy to influence, and thus direct, the richness-plant nutrients, and high level of mycotrophy making it an ideal host for productivity relationship. studies to assess the functional variability of AMF. Therefore, the Great functional variability of AMF has been detected, both aim of this work was to evaluate the functional variability, both regarding species and isolates of the same species defined based on among the species of different genera and different isolates of the spore morphology (Avio et al., 2006; Munkvold et al., 2004; Smith same species of AMF, regarding root colonization, growth effects, et al., 2004). However, these studies evaluated a small number of and phosphorous uptake of corn, Zea mays L. (Poaceae). isolates of a single genus (Glomus). The present study is the first to assess a large number of isolates, encompassing various species 2. Material and methods and genera from tropical ecosystems, regarding their functional variability in relation to a single plant species. 2.1. Fungal material In general, the symbiotic efficiency of an AMF isolates is attributed to two main factors: the ability to abundantly colonize A total of 42 AMF isolates belonging to 20 species and 8 the roots and the ability to promote beneficial responses for the genera were used in this study (Table 1). Initially, to reduce the Table 1 List of the AMF isolates studied in this work. a a b c Family Species Code of origin Code Plant of origin Location of origin Biome of origin Institution d of origin Acaulosporaceae Acaulospora colombiana A87 (CNPAB 043) Ac1 Gleichenia sp. Itumirim, MG Cerrado CNPAB Acaulosporaceae Acaulospora colombiana A15 (CNPAB 015) Ac2 Zea mays Barra do Piraí, RJ Atlantic forest CNPAB Acaulosporaceae Acaulospora colombiana ALCOA-CCB2 Ac3 – Minas Gerais Cerrado UFLA Acaulosporaceae Acaulospora colombiana 06-UFLA Ac4 – – – UFLA Acaulosporaceae Acaulospora colombiana AMZ570A Ac5 – Benjamin Constant, AM Amazon forest FURB Acaulosporaceae Acaulospora morrowiae 401-UFLA Am1 Native grasses Três Marias, MG Cerrado UFLA g e Acaulosporaceae Acaulospora scrobiculata A38 (IES-33) As1 – IES (Cuba) – CNPAB Acaulosporaceae Acaulospora scrobiculata ALCOA29 As2 – Poc¸ os de Caldas, MG Atlantic forest UFLA Acaulosporaceae Acaulospora spinosa 95-UFLA Asp – – Cerrado UFLA Acaulosporaceae Acaulospora sp. A88 (CNPAB 044) Aca Gleichenia sp. Itumirim, MG Cerrado CNPAB Claroideoglomeraceae Claroideoglomus etunicatum 365-UFLA Ce1 Coffea arabica Patrocínio, MG Cerrado UFLA Claroideoglomeraceae Claroideoglomus etunicatum URM-FMA 03 Ce2 – – – UFPE Claroideoglomeraceae Claroideoglomus etunicatum – Ce3 – Santa Catarina – ESALq Claroideoglomeraceae Claroideoglomus etunicatum SCT101A Ce4 Malus domestica Santa Catarina Pinhais forest FURB Glomeraceae Glomus formosanum A20 (CNPAB 020) Gf Imperata brasiliensis Barra do Piraí, RJ Atlantic forest CNPAB f Glomeraceae Rhizophagus clarus A5 (CNPAB 005) Rc1 – INVAM – CNPAB Glomeraceae Rhizophagus clarus URM-FMA 08 Rc2 – – – UFPE Glomeraceae Rhizophagus clarus CMM-306 Rc3 Native grasses Três Pontas, MG Cerrado UFLA Glomeraceae Rhizophagus clarus – Rc4 – Florianópolis, SC – ESALq Glomeraceae Rhizophagus clarus 351-UFLA Rc5 – Flórida, EUA – UFLA Glomeraceae Rhizophagus clarus A90 (CNPAB 046) Rc6 Canavalia rosea Recife, PE Planície costeira CNPAB Glomeraceae Rhizophagus manihotis A83 (CNPAB 041) Rm Manihot esculenta Seropédica, RJ Atlantic forest CNPAB Gigasporaceae Gigaspora albida URM-FMA 01 Gia1 – – – UFPE Gigasporaceae Gigaspora albida 03-UFLA MG Gia2 Native grasses Três Marias, MG Cerrado UFLA e Gigasporaceae Gigaspora candida A36 (IES-29) Gic1 – IES (Cuba) – CNPAB h Gigasporaceae Gigaspora candida BEG17 Gic2 – Taiwan Tropical BEG agricultural Gigasporaceae Gigaspora margarita A49 (Inóculo 138) Gim1 Coffea arabica Patrocínio, MG Cerrado CNPAB Gigasporaceae Gigaspora margarita A1 (CNPAB 001) Gim2 –